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SAGE-Hindawi Access to ResearchParkinson’s DiseaseVolume 2010, Article ID 263083, 6 pagesdoi:10.4061/2010/263083

Research Article

The Impact of Clinical and Cognitive Variables onSocial Functioning in Parkinson’s Disease: Patientversus Examiner Estimates

Patrick McNamara,1 Karina Stavitsky,2 Raymon Durso,1 and Erica Harris1

1 Department of Neurology, Boston University School of Medicine and VA New England Healthcare System,72 East Concord Street, B528, Boston, MA 02118, USA

2 Department of Psychology, Boston University, Boston, MA 02215, USA

Correspondence should be addressed to Patrick McNamara, [email protected]

Received 14 July 2009; Revised 18 December 2009; Accepted 9 February 2010

Academic Editor: Marjan Jahanshahi

Copyright © 2010 Patrick McNamara et al. This is an open access article distributed under the Creative Commons AttributionLicense, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properlycited.

Purpose. To assess the impact of clinical variables on social skills and behaviors in Parkinson’s disease (PD) patients and patientversus examiner estimates of social functioning. Methods. Twenty-eight patients with PD and 32 controls with chronic disease wereassessed with a battery of neuropsychologic, personality, mood, and social function tests. Results. Patients’ estimates of their ownsocial functioning were not significantly different from examiners’ estimates. The impact of clinical variables on social functioningin PD revealed depression to be the strongest association of social functioning in PD on both the patient and the examinerversion of the Social Adaptation Self-Evaluation Scale. Conclusions. PD patients appear to be well aware of their social strengthsand weaknesses. Depression and motor symptom severity are significant predictors of both self- and examiner reported socialfunctioning in patients with PD. Assessment and treatment of depression in patients with PD may improve social functioning andoverall quality of life.

1. Introduction

A series of recent studies suggest that patients withParkinson’s disease (PD) present with impairments in socialbehaviors and social functioning [1–4]. Changes in thequality of social interactions, furthermore, may predate onsetof overt extrapyramidal motor signs of PD by several years[5, 6]. Thus, a better understanding of the determinants ofsocial functioning in PD is needed.

Deficits in executive cognitive functions that are oftenassociated with PD [7] may also influence social func-tioning and self-monitoring of social behaviors. Specificpersonality and behavioral changes are often observed inpatients with deficits in frontal lobe functioning. Thesepersonality changes include problems with behavioral disin-hibition, apathy, disinterest, interpersonal communication,and irritability [1, 8–11]. Patients who present with executive

deficits and personality changes associated with these deficitswould likely also evidence impairments in social functioningsuch as those related to social interactions and empatheticresponding.

Mood and general cognitive function may also be factorsthat influence social functioning. For example, patients whoare depressed often show impaired social behaviors [12]and show improvements in a variety of social domainsafter treatment with antidepressant medication [13]. It isalso likely that clinical factors such as disease severity,mood and cognitive dysfunction will negatively impact socialfunctioning in PD.

To date, no studies have simultaneously assessed effectsof patients’ own awareness of social functioning or of theimpact of clinical, cognitive and personality variables onsocial functioning in PD. In the following study, we evaluatedsocial functioning in PD by simultaneously assessing the

2 Parkinson’s Disease

contribution of several clinical variables to both self-reportedand examiner-rated social behaviors (including social func-tioning and empathy) in PD.

2. Methods

The study was approved by the Veterans Affairs (VA) InternalReview Board for protection of human subjects. One ofthe authors (Erica Harris) presented each participant with adetailed informed consent agreement that described the risksand procedures of the study. After the participant indicatedconsent and signed the form, testing began.

2.1. Participants. Twenty-eight nondemented patients withPD (2 female) were recruited from the outpatient MovementDisorders Clinic at the VA Boston Healthcare System,Boston, MA. Patients were individually diagnosed by Dr.Raymon Durso, director of the clinic. All were right-handed.Ten patients were at Hoehn-Yahr (H-Y) Stage II and 15 atStage III. All patients were rated for disease severity on theUnified Parkinson’s Disease Rating Scales (UPDRS) by a PDspecialist (Raymon Durso). All participants scored 25 andabove on the Mini-Mental State Examination [14] and nonewere demented according to clinical examinations and DSM-IV [15] criteria. All were on some form of dopaminergicmedication and were tested while on medications withoptimal effects (i.e., motor signs were well controlled).Medication information was obtained from each patientby the neurologist and levodopa equivalent dosages werecalculated based on previous reports with 100 mg levodopa =83 mg levodopa with a COMT inhibitor = 1 mg pramipexole= 1 mg pergolide [16]. Thirty-two control subjects (CS; 12female) were also recruited from the VA community. All ofthese control participants had some form of chronic diseaseor medical complaint such as low back, head or neck chronicpain syndromes. All participants with a history of substanceabuse or head injury were excluded.

3. Measures

3.1. Mood Tests. We assessed depression, stress and anxietywith the short-form of the Depression Anxiety Stress Scales(DASS) developed by S.H. Lovibond and P.F. Lovibond[17]. Crawford and Henry [18] and Antony et al. [19]have reported excellent reliability, validity and otherpsychometric properties for the three subscales of the DASS.The test includes 21 questions, 7 in each of the depression,anxiety and stress subscales with higher scores indicatinggreater impairment. The DASS Manual [17] reports thefollowing cutoff scores for depression (normal = 0–9, mild= 10–13, moderate = 14–20, severe = 21–27, and extremelysevere = 28+); anxiety (normal = 0–7, mild = 8–9, moderate= 10–14, severe = 15–19, and extremely severe = 20+),and stress (normal = 0–14, mild = 15–18, moderate =19–25, severe = 26–33, and extremely severe = 34+). TheDASS Manual indicates that the scores of the DASS21 arecomparable to the scores of the full length DASS but thatthe scores will need to be doubled before comparison to

the cutoff scores. The DASS Manual also reports Cronbach’salpha-coefficients for each of the 3 subscales: depression =0.81, Anxiety = 0.73 and Stress = 0.81 [17].

3.2. Stroop Color-Word Interference Procedure. To assessexecutive cognitive functioning, we used the Stroop color-word interference test. This test requires the subject to namethe color of the ink or to name the word of a color-word thatis printed [20]. An “interference” test card consists of rowsof color words printed in ink colors incongruent with theword represented, with the task being to name the ink colorsas quickly as possible. Susceptibility to cognitive interferenceis calculated as the total time taken to name the colorsand read the words. PET studies show that orbitofrontalcortex is activated in healthy subjects during the interferencecondition [21].

3.3. Social Adaptation Self-Evaluation Scale (SASS). To quan-titatively assess quantity and quality of overt social behaviors,we used the Social Adaptation Self-Evaluation Scale (SASS).The SASS [13] is a 21-item questionnaire that is administeredto patients (SASS-P) to obtain self-ratings about behaviorand motivation. A virtually identical version of the question-naire is provided to the examiner or to a significant other(SASS-E) to fill out with respect to the patient. The itemstarget specific types of social behavior. We required the raterto rate the quality of those behaviors and if they occur at all.“Quality” refers to how well the social behavior is adaptedto social context and how well the behavior accomplishesintended goals of the patient. Ratings for each social behaviorrange from 0–3 (0 = no, 1 = minimal, 2 = medium, and3 = maximal social adjustment). The minimum score forboth the self-report and examiner versions of the scale is0 and the maximum score is 60. Higher scores indicategreater adaptation to the social environment. Using thisscale, “normal” social functioning was determined to be ascore of 35–52; therefore, impaired functioning is any scorebelow 35. The SASS evidences good face validity, internaland external validity, test-retest reliability, and a Cronbach’salpha-coefficient of 0.74 for all individual items [13].

3.4. Empathy Quotient. The ability to empathize withanother is a core social ability as it allows one to takethe perspective of another in any given social exchange.To assess interpersonal empathy ability, we administered anempathy scale devised by Baron-Cohen and Wheelwright,The Cambridge Behaviour Scale [22]. It contains a total of60 self-report statements with only 40 of those statementstapping empathy and the remaining 20 statements acting asfillers. About half of the statements were worded to producedisagree responses so that biased responding sets could bechecked. The empathy scale yields an “empathy quotient”, orEQ. The minimum EQ score is 0 and the maximum scoreis 80, with one point given if the empathic statement isendorsed mildly (slightly agree) or two points given it if isendorsed strongly (strongly agree). The same scoring rulesapplied to those empathic statements that elicited a “strongly

Parkinson’s Disease 3

Table 1: Comparison of clinical and demographic variables in CS and PD participants.

CS (n = 32) PD (n = 28) Significance

Age 56.3 (9.2) 66.5 (11.9) P < .0001∗∗∗

Education 15.3 (2.7) 13.9 (3.0) ns

MMSE 28.3 (1.5) 26.6 (1.7) P < .0001∗∗∗

DASS—Anxiety 2.12 (2.4) 5.32 (4.1) P < .0001∗∗∗

DASS—Depression 3.94 (4.7) 4.32 (4.3) ns

Stroop 3 Interference 46.8 (29.8) 51.3 (29.8) ns

Disease Duration N/A 9.01 (4.96) N/A

H and Y Stagea N/A 3 (2–3) N/A

UPDRS total N/A 25.3 (13.1) N/A

LDE N/A 628.9 (330.8) N/A

Notes: ∗∗∗P < .0001; ns: not significant; N/A: not applicable; CS: control; PD: Parkinson’s disease; MMSE: mini-mental state exam; DASS: Depression AnxietyStress Scales; H & Y Stage: Hoehn & Yahr Stage; UPDRS: Unified Parkinson’s Disease Rating Scale; LDE: Levodopa Dosage Equivalent.aMedian (range) is reported.

Table 2: Comparison of CS and PD participants on SASS and EQ variables.

CS (n = 32) PD (n = 28) Significance

SASS-P total 42.8 (10.7) 40.4 (7.6) ns

SASS-E total 44.6 (11.1) 41.4 (9.7) ns

EQ Total 40.7 (12.7) 39.3 (12.3) ns

Notes: ns: not significant; CS: control; PD: Parkinson’s disease; SASS-P: Social Adaptation Self-Evaluation Scale, Patient version; SASS-E: Social AdaptationSelf-Evaluation Scale, Examiner version; EQ: The Cambridge Behaviour Scale, empathy quotient.

disagree” or “slightly disagree” responses [23]. Test-retestreliability for the EQ is r = 0.97 [22].

4. Statistical Analyses

4.1. The Social Functioning Data in Both the CS and thePD Participants Was Normally Distributed. Independentstudent’s t-tests were performed to compare differencesbetween CS and PD groups on all demographic and clinicalvariables as well as variables related to social functioning.Paired-samples t-tests were performed in order to examinedifferences between patient and examiner report of socialfunctioning in both PD and CS groups. A multiple regressionanalysis was performed to examine which clinical andcognitive variables significantly accounted for variance inpatient and examiner ratings of social functioning as well asinterpersonal empathy. The analyses were performed usingDASS-anxiety, DASS-depression, age, disease stage, diseaseduration, UPDRS total, MMSE and Stroop interference aspredictors and SASS-P, SASS-E, and EQ as the criterionvariables.

5. Results

Demographic and clinical differences between PD and CSparticipants are presented in Table 1. PD participants weresignificantly older, had lower MMSE scores and had higherDASS total scores. We therefore treated these latter threevariables (age, MMSE score and mood) as covariates in allthe analyses that follow.

5.1. Overall Differences in Social Functioning and Empathyin PDs versus Controls. No significant differences in socialfunctioning or empathy score were found between PD andCS participants, even when controlling for age, MMSE andDASS total mood score (see Table 2).

5.2. Examiner versus Patient’s Ratings on the SASS. Therewere no significant differences on any of the individual SASSitems or on the total scores between examiner and self-reportof social functioning in either PD or CS groups.

5.3. Predictors of Examiner Estimates on Patient SocialFunctioning. The next set of analyses was performed toexamine the relationship of clinical variables to examiner’sestimates of patient social functioning (see Table 3). Theoverall model was significant accounting for 73% of variancein SASS-E score. When each variable was examined, DASS-depression was the only significant predictor of socialfunctioning in patients with PD as reported by the observers(β = −.67,P = .002).

5.4. Predictors of Patient’s Self-Rankings on Social Behaviors.This analysis was repeated for the patient version of the SASSand again the overall model was significant accounting for75% of variance in SASS-P score (Table 3). For this versionof the SASS, DASS-depression was the strongest predictor ofpatient self-rating of their social functioning (β = −.60,P =.004) followed by UPDRS total (β = −.44,P = .04).

5.5. Predictors of Interpersonal Empathy. A third set ofmultivariate regression analyses was performed to examine


Table 3: Results of multiple regression analyses of clinical variables as predictors of social functioning in patients with PD. Values presentedare the standardized coefficient Beta (β) and P-values for SASS-E, SASS-P, and EQ.

β (P value)

SASS-E SASS-P EQ

Disease Duration −.31± .28 (P = .06) .16± .22 (P = .34) −.33± .48 (P = .13)

Disease Stage −.06± .59 (P = .66) −.12± .46 (P = .43) −.16± .83 (P = .42)

UPDRS Total −.27± .14 (P = .18) −.44± .11 (P = .04)∗ −.38± .25 (P = .15)

MMSE .32± 1.56 (P = .10) −.30± 1.23 (P = .14) −.30± 2.66 (P = .25)

Age −.04± .13 (P = .79) −.09± .10 (P = .60) .11± .22 (P = .62)

DASS Anxiety −.11± .46 (P = .56) −.16± .37 (P = .41) −.12± .79 (P = .65)

DASS Depression −.67± .42 (P = .002)∗∗ −.60± .33 (P = .004)∗∗ −.28± .71 (P = .27)

Stroop Interference .14± .07 (P = .52) −.08± .05 (P = .71) −.54± .12 (P = .08)

Notes: ∗P < .05; ∗∗P < .01; SASS-E: Social Adaptation Self-Evaluation Scale, Examiner version; SASS-P: Social Adaptation Self-Evaluation Scale, Patientversion; EQ: The Cambridge Behaviour Scale, empathy quotient; MMSE: mini-mental state exam; DASS: Depression Anxiety Stress Scale; UPDRS: UnifiedParkinson’s Disease Rating Scale.

the impact of the same set of clinical variables (DASS-anxiety, DASS-depression, age, disease stage, disease dura-tion, UPDRS total, MMSE, and Stroop interference) on thetotal score on the EQ (see Table 3). These analyses revealedthat none of the above variables were significant predictorsof the EQ score.

6. Discussion

In the current study, we found that patients with PD andclose examiners of these individuals did not differ in ratingtheir social behaviors. PD patients appear to be well aware oftheir social strengths and weaknesses. A multivariate analysisof the impact of clinical variables on social functioning in PDrevealed that depression is the strongest predictor of socialfunctioning in PD for examiner and patient-rated scoresof social functioning. In addition, an analysis of patients’self-rating of their own social interactions also revealed thatmotor symptom severity may impact social functioning inpatients with PD. None of the clinical or cognitive variableswere significant predictors of empathy in those with PD.These findings suggest that patients estimate their socialinteraction abilities on the basis of their own experience ofdisease severity and their overall mood while close examinersrely on observed mood states of the person with PD whenjudging the quality of PD social interactions.

Social functioning requires communication of ideas andemotions between persons involved in a social interaction.Communication of emotion between people requires an abil-ity to empathize with others as well as effective conveyance ofvisual impressions, facial displays, speech prosody patternsand gesture, among other capacities. Our data suggest thatthe ability to empathize with others appears to be intactin persons with PD. Nevertheless, independent lines ofevidence [24–26] suggest that PD patients exhibit impairedrecognition of emotional expression in the faces of otherpeople. This impairment persists even after controlling forvisual discrimination deficits. Other symptoms of PD suchas masked facies and dysarthria can make communicationdifficult and thus influence the quality and quantity of social

interactions. Crucian et al. [27] reported induction of verbalkinesia paradoxica in some patients with PD who were askedto recall emotional episodes. Patients could not adequatelyexpress their memory-linked emotions. All of these factssuggest that PD patients, particularly depressed PD patients,may be impaired in the expression and recognition of socialemotions.

Patients with primary depression (without PD) have alsobeen reported to be impaired on a variety of social domains[12]. In these patients, treatment of depression is linkedto improvement in social functioning [13]. In the currentstudy, we found that in patients with PD, depression was alsolinked to greater impairment in social functioning. Almosthalf of PD patients (45%) experience clinically significantlevels of depression [28]. Depression in PD is not related tothe motor symptom severity or the duration of the disease[28]. However, it significantly reduces quality of life, and aswe document here, it impairs social interaction and socialbehaviors.

Our study has limitations. We did not assess apathywhich is a common nonmotor symptom of PD that isassociated with reduced motivation and reduced initiation ofsocial interactions. Thus, we cannot rule out the possibilitythat some of the patients had apathy and that apathy, inaddition to mood and motor deficits, was influencing socialoutcomes. We also used a small convenience sample, andtherefore, our participants may not be representative of thelarger PD population. PD is heterogeneous in its presentationand a small sample may not sufficiently represent the varioussymptom profiles of patients in the general population.Because of its heterogeneity, various studies have aimed toinvestigate meaningful subtypes of the disease, an effort thatis important for understanding the etiology of the disorderand disease management. Due to the sample size limitationand lack of power we were not able to analyze subgroupsof patients, which would give a more thorough examinationof the association of depression and social functioning. Alarger scale study is therefore needed to investigate thisissue more thoroughly. The current study did not includeany diagnostic measures of depression so we were not able

Parkinson’s Disease 5

to examine whether patients who were clinically depressedpresented with deficits in social functioning. However, ourstudy demonstrates that higher scores on a measure ofdepression do significantly predict lower scores on a measureof social functioning. Future research is needed to more thor-oughly investigate the contribution of clinically diagnoseddepression to social functioning in PD. In addition, we didnot measure all relevant variables for an analysis of socialfunctioning in PD. A key aspect of social cognition is theability to infer other peoples’ mental states, thoughts andfeelings. This is referred to as Theory of Mind (ToM), ormentalizing ability. We did not measure ToM abilities in ourparticipants so we could not assess the potential impact ofToM performance on social skills in PD. To our knowledge,only two studies have been published on ToM abilities in PD[4, 29]. Both studies reported that PD patients were impairedon at least one ToM task.

In summary, this study suggests that both the awarenessof and social dysfunction itself in PD may be a function ofvarious disease-related factors such as depression and motorsymptom severity. Treating the depression may improvesocial functioning and improve quality of life in thesepatients. Various studies show that pramipexole improvesdepression in addition to motor symptoms in patients withPD [28]. By studying the social cognitive abilities of patientsand the relation of these to other clinical characteristics ofthe disease, we have for the first time quantitatively describedelements of social interaction in PD in relation to well-defined clinical factors, an area previously neglected in earlierstudies of behavioral impairment in PD.

Acknowledgments

This material is based upon work done and supported, inpart, by the Office of Research and Development, Medi-cal Research Service, Department of Veterans Affairs andNIDCD Grant no. 5R01DC007956-03.

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